Sputum bacteriology in patients with acute exacerbations of COPD in Hong Kong

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1 Respiratory Medicine (2005) 99, Sputum bacteriology in patients with acute exacerbations of COPD in Hong Kong Fanny W.S. Ko a, Tony K.C. Ng b, Thomas S.T. Li c, Joan P.C. Fok a, Michael C.H. Chan a, Alan K.L. Wu a, David S.C. Hui a, a Department of Medicine and Therapeutics, Prince of Wales Hospital, Chinese University of Hong Kong, Ngan shing Street, Shatin, New Territories, Hong Kong b Department of Microbiology, the Chinese University of Hong Kong, Hong Kong c Department of Anaesthesia and Intensive Care, The Chinese University of Hong Kong, Hong Kong Received 15 June 2004 KEYWORDS Chronic obstructive pulmonary disease; Exacerbation; Sputum; Bacteria Summary Study objective: To study the demographics and sputum microbiology of patients admitted to a teaching hospital with acute exacerbations of chronic obstructive pulmonary disease (AECOPD). Design: A retrospective study. Setting: A tertiary university hospital in Hong Kong. Patients: All episodes of AECOPD, patient demographics, length of stay, sputum culture and radiological results admitted in the first half of the year 2000 were retrieved from hospital records. Results: There were 329 patients with 418 episodes of AECOPD without concomitant pneumonia. The age of the patients was years. The acute hospital length of stay for an episode of AECOPD was days. Haemophilus influenzae was the commonest organism found in sputum (23.1%), followed by Pseudomonas aeruginosa (6.3%) and Streptococcus pneumoniae (4.0%). Mycobacterium tuberculosis was found in 1.1% of the admissions. Presence of organisms in sputum had no association with the hospital length of stay and intensive care unit admissions. In patients whose FEV 1 was 450% of predicted values, there was a higher chance of positive sputum growth of H. influenzae than those with FEV 1 o50% (16/ 44 vs. 31/162 episodes, respectively, P ¼ 0:02). Conclusions: H. influenzae was the commonest bacterium isolated in sputum in patients with AECOPD. In areas endemic of tuberculosis, it is advisable to use fluoroquinolones for AECOPD with caution. & 2004 Elsevier Ltd. All rights reserved. Abbreviations: AECOPD, acute exacerbation of COPD; CAP, community acquired pneumonia; CXR, chest radiograph; TB, pulmonary tuberculosis Corresponding author. Tel.: ; fax: address: dschui@cuhk.edu.hk (D.S.C. Hui) /$ - see front matter & 2004 Elsevier Ltd. All rights reserved. doi: /j.rmed

2 Acute exacerbations of COPD 455 Introduction Chronic obstructive pulmonary disease (COPD) is a common disease worldwide with a significant morbidity and it incurs heavy utilization of healthcare resources. In Hong Kong, COPD was the fourth leading cause of death, and accounted for 3% of all public hospital admissions in The prevalence of chronic bronchitis and emphysema was estimated to be 7% and 2%, respectively among those aged 70 years or over in the general population in Hong Kong. 1 Previous studies have shown that pulmonary function and quality of life were adversely affected by frequent exacerbations, particularly in active smokers. 2,3 Infectious agents are recognized as a major pathogenic factor in exacerbations. Other contributing factors for exacerbation include air pollution, low temperature and interruption of regular treatment. 4 6 In community-acquired pneumonia (CAP), the organisms responsible for the infection varied in different parts of the world. In most countries, Streptococcal pneumoniae and Haemophilus influenzae were the major organisms responsible for CAP. Legionella pneumophila, which was estimated to be the responsible etiological agent for CAP in 2 8% in North America, was an infrequent cause of pneumonia in Asian countries like Japan. 7,8 Current data on bacteriology related to acute exacerbations of COPD (AECOPD) were mainly derived from the western countries There are very few data on this aspect within the Asian Pacific region. As our spectrum of organisms might be different from those of other countries or regions, it is important to examine the bacteriology responsible for AE- COPD, which has important therapeutic implication for the choice of empirical antibiotic treatment for this common condition. Thus the aims of this study were to examine the background, clinical manifestations, and infectious etiologies in the sputum specimen in relation to clinical outcome in patients admitted with AECOPD in Hong Kong. Methods This was a retrospective study based on review of data from patients who were admitted with AECOPD to the Prince of Wales Hospital (an acute hospital in Hong Kong serving a population of 600,000) from January to June Patients were identified from the hospital database by International Classification of Diseases 9th Revision Clinical Modification Codes (ICD-9-CM). 14 Patients with the code numbers and 496 were selected (as the principle diagnosis or other diagnosis). These codes included the diagnosis of acute bronchitis with chronic obstructive pulmonary disease, acute and chronic obstructive bronchitis, acute exacerbation of chronic obstructive pulmonary disease and chronic airway obstruction, not elsewhere classified. Hospital records were then retrieved and reviewed by the investigators. All patients with sputum specimen saved for investigations were included in the study (including routine culture and mycobacterial culture). When reviewing the case notes, AECOPD would be considered if the patient had background COPD with at least two of the major symptoms (increased dyspnoea, increased sputum purulence, increased sputum amount) or one major and one minor symptom (nasal discharge/congestion, wheeze, sore throat, cough). 2,15 Detailed information on the COPD exacerbations was collected from the case records. Information collected included the demographic data, radiological results, sputum culture results, blood test results, lung function test data, length of stay in hospital and number of readmissions over 1 year from the first exacerbation in the study period. Lung function data of the patients were collected from their medical records when the patients were free of acute exacerbations (spirometry at clinic follow up, either before or after the exacerbation, within 1 year). All the recorded spirometry tests were performed in our pulmonary function laboratory meeting the standards required by the American Thoracic Society. 16 Chest radiograph (CXR) findings were evaluated by the investigators. Patients who had new infiltrates on the CXR were considered to have pneumonia rather than pure COPD exacerbations and thus would not be included in the study. Expectorated sputum was collected into a sterile container and processed according to standard procedures. 17 Microscopy by Gram staining was performed for presence of leucocytes, epithelial cells and organism morphotypes. Specimens with more than 10 epithelial cells per low power field were not cultured unless the specimen appeared purulent or bloodstained. After homogenization with sputolysin, quantitative culture was performed using a 1 ml standard loop onto blood agar and chocolate blood agar plates which were incubated in 5% CO 2 at 35 1C for h. Culture plates were reincubated for a further 24 h if there was no growth after overnight incubation or predominant morphotype seen in Gram smear had not yet been isolated. Common lower respiratory tract pathogens (e.g. S. pneumoniae, H. influen-

3 456 zae, Morexella catarrhalis) were reported semiquantitatively when isolated. Only isolates with higher than 10 5 colony forming units were reported as a positive growth. Potential pathogens (including Pseudomonas spp. Klebsiella and other Enterobacteriaceae spp., Staphylococcus aureus, Candida spp., Pasteurella spp., b-haemolytic streptococci, etc.) were reported only when they were present in heavy or predominant growth, or in the absence of oral commensals. Acid fast staining and culture for Mycobacterium species onto Lowenstein Jensen medium after decontamination of sputum specimens were performed according to standard procedures. 18 Statistics Data were analyzed by the Statistical Package of the Social Science (SPSS) Statistical software for Window, Version 10.0 (SPSS Inc., IL, USA). The association between the presence of bacteria in sputum, the background characteristics and clinical outcomes of patients (length of hospitalization, number of readmissions over 1 year period and ICU admissions) was assessed by Mann Whitney U test, chi-square test and Fisher s exact test as appropriate. Data were presented as mean7sd unless otherwise stated. A P value of less than 0.05 was considered as significant. Results A total of 711 episodes of COPD exacerbations (534 patients) were identified from computer records from January to June Case records were retrieved but the records of 18 episodes (10 patients) were missing. In the case records reviewed, 574 episodes were related to COPD exacerbations among 452 patients. Among these, 150 episodes (118 patients) had pneumonic changes on CXR whereas 418 episodes (329 patients) had no pneumonic changes on CXR. Six episodes (5 patients) did not have the X-ray changes documented in case records. Only the 418 episodes without pneumonic changes on CXR were included in this study. Demographic data of the subjects are shown in Table 1. The average age of the patients was above 70 years with the majority being males (78.7%) and ex-smokers (82.1%). Among these patients, 53.3% had lung function tests performed at stable state within 1 year of the first admission for the AECOPD in the study period. The mean FEV 1 was % predicted. Only 21.0% of the patients Table 1 Demographic data of patients admitted with COPD exacerbation (first admission in the study period) (n ¼ 329). Age Sex (M/F) 259/70 Smoking status Smokers 50 (15.2) Ex-smokers 270 (82.1) Non-smokers 8 (2.4) Social support Lives with family 257 (78.1) Home alone 30 (9.1) Lives in institution 36 (10.9) Activities of daily living Can climb at least 1 2 flight of 89 (27.1) stairs Outgoing but level ground 149 (45.3) exercise tolerance Homebound 72 (21.9) Chairbound 11 (3.3) Use of home O 2 76 (23) Use of non-invasive home ventilation 4 (0.12) Lung function (n ¼ 172) FEV 1 percentage predicted Medication use Using ICS 66 (20.1) Using theophyllines 87 (26.4) Data presented as mean7sd (percentage). F.W.S. Ko et al. were on inhaled corticosteroids (ICS) whereas 26.4% were taking oral theophylline before hospitalization. Clinical data of patients admitted to hospital with AECOPD are shown in Table 2. The average length of stay in the acute hospital was 7 days. Fever ( C) was present in 16.7% of the episodes. White cell count of X /L was present in 45.7% of the exacerbations. The number of re-admissions to hospital within 1 year from the first admission in the study period was times. The mortality rate of the patients within one year was 14.0%. Among all the episodes of AECOPD, 151(37.8%) had positive results on routine sputum the three most common organisms grown in sputum culture for patients with AECOPD were H. influenzae (23.1%), P. aeruginosa (6.3%) and S. pneumoniae (4.0%). The routine sputum culture results are shown in Fig. 1. Mixed infections were identified in

4 Acute exacerbations of COPD 457 routine sputum cultures in 53 (13.3%) episodes of AECOPD. Readmissions were not caused by the same previously detected strain of bacteria in the majority of cases. Only five episodes out of the 70 re-admissions with pure AECOPD (three had H. influenzae, two had Pseudomonas aeruginosa whereas 1 had S. pneumonia) had the same organism grown in sputum in the subsequent admissions as the first admissions. Mortality had no correlation with positive sputum cultures, either as a whole or with each individual organism. Concerning the resistance pattern of the common organisms, beta-lactamase activity was found in 31 out of 92 (33.7%) isolates of H. influenzae. At Table 2 Clinical data of patients admitted with acute exacerbation of COPD (by episodes)(n ¼ 418). Hospital stay in acute hospital (days) Hospital stay in convalescent hospital (days) Fever on admission 70 (16.7) WCC on admission ICU admission 11 (2.6) Use of NIPPV 34 (8.1) Use of mechanical ventilation 8 (1.9) Data presented as mean7sd (percentage); NIPPV: noninvasive mechanical ventilation; ICU: intensive care unit; WCC: total white cell count ( 10 9 /L). least intermediate resistance to penicillin was identified in 4 out of 16 (25%) of S. pneumoniae isolates. The mycobacterial culture results are shown in Fig. 2. A total of nine (2.6%) patients had positive mycobacterial sputum culture when admitted to hospital with AECOPD. Among these patients with positive mycobacterial growth, M. tuberculosis (MTB) was identified in four (1.1%) patients whereas atypical mycobacterium was identified in five (1.4%) of the admissions. The atypical mycobacteria included M. chelonae, M. kanassi and M. fortuitium. Only one patient had positive sputum growth on both routine culture (Enterobacter) and mycobacterial culture (M. tuberculosis). The positive growth of H. influenzae, P. aeruginosa and S. Pneumoniae in the sputum specimen was found to have no association with the patients length of hospitalization, number of re-admissions over 1 year, number of admissions for COPD over the past year, ICU admissions, age of patients, activities of daily living, and co-morbidities such as congestive heart failure. Analysis of the relationship between lung function and presence of bacteria in sputum was performed in the 206 episodes where lung function data were available. In patients whose FEV 1 was 450% predicted, there was a higher chance of positive sputum growth of H. influenzae than those with FEV 1 o50% (16/44 vs. 31/162 episodes, respectively, P ¼ 0:02). However, no correlation between other individual organisms or presence of any organisms with lung function (using an Percentages H. influenzae P. aeruginosa S.. Pneumoniae M. catarrhalis Klebsiella Acinetobactor Stenotrophomonas S.. Aureus Coagulase -ve staph. MRSA Enterobacter Proteus Bacteria Figure 1 Bacterial flora in sputum of patients with acute exacerbation of COPD.

5 458 F.W.S. Ko et al. Percentages Mycobacterial TB Mycobacteria Other mycobacterium Figure 2 Mycobacterial growth from sputum of patients with acute exacerbation of COPD. arbitrary FEV 1 cut off value of 50% of predicted values) was observed. If the FEV 1 cut off value was taken as 30% of predicted values (76 episodes had FEV 1 o30% and 130 episode had FEV 1 X30% predicted normal), no correlation between bacterial growth and lung function was observed. Discussion This retrospective study described the demographics, clinical manifestations and infectious etiologies in the sputum collected from patients who had been admitted to hospital with AECOPD in Hong Kong. We found that 37.8% of our patients with AECOPD had a positive routine sputum culture. In addition, M. tuberculosis was detected on sputum culture in 1.1% of them. In patients whose FEV 1 was 450% of the normal predicted values, a higher chance of positive growth of H. influenzae from the sputum was observed. A prospective study in Netherlands over a 1-year period found that 50% of patients admitted to hospital with AECOPD had positive sputum culture. Pathogens more frequently isolated were H. influenzae (45%), S. pneumoniae (27%), and P. aeruginosa (15%). 9 Similarly, two multi-center studies in Spain found that about half of the patients with AECOPD requiring hospitalizations had positive sputum culture. 12,13 Similar to other studies, 9,12 H. influenzae was the commonest organisms (23.1%) identified on the sputum culture in our study. A substantial number of our patients had P. aeruginosa detected in the sputum though the percentage (6.3%) was lower than other reports with a prevalence rate of about 15%. 9,12 A previous study found that poor airway function, defined as FEV 1 o50%, was associated with P. aeruginosa and H. influenzae isolation from sputum. 12 Groenewegen and Wouters 9 also observed that the proportion of patients with bacterial infection was higher in those with FEV 1 o50% predicted. However, they did not identify a positive relationship between the type of bacteria and lung function. In contrast, we noted that H. influenzae was found more commonly in patients whose FEV 1 was 450% of predicted normal values than those with lower level of lung function. This observation was different from previous studies. The study by Miravitlles et al. 12 involved ambulatory patients in clinics rather than patients with AECOPD requiring hospitalizations as in our study. The study of Groenewegen et al. also involved patients with AECOPD who required hospitalization. Their patients also had comparable lung function with our group of patients. However, the study of Groenewegen was of prospective design whereas ours was a restropective study. As there are only sparse amount of data in the medical literature on the relationship between sputum bacteriology and lung function, more studies are needed to assess the pattern of bacterial infection in relation to lung function results. M. tuberculosis was isolated from sputum in 1.1% of our patients admitted with AECOPD. A study in Hong Kong in the 1990s estimated that 12% of patients admitted to hospital with CAP suffered from M. tuberculosis infection. 19 Hong Kong has had a high prevalence of pulmonary tuberculosis (TB). In the year 2003, the TB notification rate was 89.2 per 100,000 population. 20 Screening for TB in patients with AECOPD is essential in this locality with a high background prevalence of TB infection as systemic steroid is often prescribed for AECOPD in order to speed up recovery of airway function and reduce hospital length of stay. 21,22 Early diagnosis and treatment of TB infection is important in preventing spread of the disease in the community. One should also be cautious about the use of fluoroquinolones as empirical antibiotic for treatment of AECOPD or community acquired

6 Acute exacerbations of COPD 459 pneumonia in areas with a high prevalence of TB infection as this may result in delay in the diagnosis and treatment of TB infection. 23 Atypical mycobacterium was cultured from the sputum in 1.4% of our patients with AECOPD. It is possible that some of our patients might have post- TB bronchiectasis, which was not easily detected on plain chest radiographs. Atypical mycobacterial growth in sputum of these patients might be due to colonization rather than genuine infection. Nevertheless, careful follow-up with repeated sputum cultures and chest radiographs and CT scans is needed in these patients. 24 In our study, expectorated sputum was used to assess infection associated with AECOPD. The possibility of contamination by saprophytic oropharyngeal flora was a concern. However, with adherence to strict cytological criteria for reporting, it was suggested that culture of expectorated sputum could reflect the bacterial flora of the lower airway secretions. 25,26 Tools like protected specimen brush could avoid contamination of oropharngeal secretions. However, these methods were invasive and would inflict more discomfort to patients who already were suffering from AECOPD. Many studies thus still recommend this easy-toobtain and non-invasive method of expectorated sputum for assessment of the bacteriology in the airway. 12,13,27 In fact, the etiological agents identified for AECOPD were similar to those studies using invasive methods like protected specimen brush and non-invasive methods with expectorated sputum. 12,28 It has been noted that bacterial colonization may occur in patients with stable COPD. Patel et al. found that 51.7% of COPD patients at stable state had possible pathogens colonized in their lower airway as detected by sputum induction. 15 Thus identification of positive sputum culture does not necessarily indicate an infection. As sputum for routine bacterial culture was used to assess the infectious etiology, the role of atypical infectious agents like Mycoplasma pneumoniae, Chlamydia pneumoniae and respiratory viruses could not be assessed. As long as one is aware of the limitations of expectorated sputum in assessing COPD, its collection can be useful for analyzing bronchial infections. This retrospective study assessed the sputum bacteriology in patients admitted to hospital with AECOPD without radiological evidence of pneumonia. While some investigators believe that patients with concomitant pneumonia and COPD should be classified as CAP rather than AECOPD, there has been no universally agreed definition for AECOPD. AECOPD has been defined as sustained worsening of the patient s condition from the stable state and beyond normal day-to-day variations that is acute in onset and may warrant additional treatment in a patient with underlying COPD. 29 According to the American Thoracic Society guideline 30 and the Global Initiative for Chronic Obstructive Lung Disease, 31 CAP is not excluded from the diagnosis of AECOPD. Some studies on AECOPD excluded patients with pneumonia, 10,32 whereas others did not. 33,34 Furthermore, for severe CAP patients that required hospitalization, COPD is the most common comorbidity. 35,36 Nevertheless, we have reported in this study only patients with non-pneumonic AE- COPD in order to avoid any ambiguity. There were several limitations in this study. This was a retrospective review but the data were well documented in the majority of cases. Only seven episodes (six patients) did not have the X-ray changes documented in the case records. Highresolution tomography of lungs was not performed routinely in patients with AECOPD and it was possible that some patients might have concomitant bronchiectasis, which could predispose to colonization with pseudomonal and atypical mycobacterial species. In summary, we have shown that Haemophilus influenzae, Pseudomonas aeruginosa, Streptococcal pneumoniae were the commonest organisms identified in our patients with AECOPD. It is essential to screen for sputum AFB and avoid the use of fluoroquinolone as firstline antibiotic therapy in COPD patients in areas endemic of TB infection. Prospective studies are needed to assess the bacteriology and the treatment outcome for patients with AECOPD. Acknowledgments The authors wish to thank Doris P.S. Chan for the statistical analysis. References 1. Lai CK, Ho SC, Lau J, et al. Respiratory symptoms in elderly Chinese living in Hong Kong. Eur Respir J 1995;8: Seemungal TA, Donaldson GC, Paul EA, Bestall JC, Jeffries DJ, Wedzicha JA. Effect of exacerbation on quality of life in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1998;157: Donaldson GC, Seemungal TA, Bhowmik A, Wedzicha JA. Relationship between exacerbation frequency and lung function decline in chronic obstructive pulmonary disease. Thorax 2002;57: Miravitlles M. Exacerbations of chronic obstructive pulmonary disease: when are bacteria important? Eur Respir J Suppl 2002;36:9s 19s.

7 460 F.W.S. Ko et al. 5. Donaldson GC, Seemungal T, Jeffries DJ, Wedzicha JA. Effect of temperature on lung function and symptoms in chronic obstructive pulmonary disease. Eur Respir J 1999;13: Jarad NA, Wedzicha JA, Burge PS, Calverley PM. An observational study of inhaled corticosteroid withdrawal in stable chronic obstructive pulmonary disease. ISOLDE Study Group. Respir Med 1999;93: Bartlett JG, Mundy LM. Community-acquired pneumonia. N Engl J Med 1995;333: Ishida T, Hashimoto T, Arita M, Ito I, Osawa M. Etiology of community-acquired pneumonia in hospitalized patients: a 3-year prospective study in Japan. Chest 1998;114: Groenewegen KH, Wouters EF. Bacterial infections in patients requiring admission for an acute exacerbation of COPD; a 1-year prospective study. Respir Med 2003;97: Soler N, Torres A, Ewig S, et al. Bronchial microbial patterns in severe exacerbations of chronic obstructive pulmonary disease (COPD) requiring mechanical ventilation. Am J Respir Crit Care Med 1998;157: Rohde G, Wiethege A, Borg I, et al. Respiratory viruses in exacerbations of chronic obstructive pulmonary disease requiring hospitalisation: a case-control study. Thorax 2003;58: Miravitlles M, Espinosa C, Fernandez-Laso E, Martos JA, Maldonado JA, Gallego M. Relationship between bacterial flora in sputum and functional impairment in patients with acute exacerbations of COPD. Study Group of Bacterial Infection in COPD. Chest 1999;116: Monso E, Garcia-Aymerich J, Soler N, et al. Bacterial infection in exacerbated COPD with changes in sputum characteristics. Epidemiol Infect 2003;131: American Hospital Association. ICD-9-CM Basic Coding Handbook for Coders. Chicago: American Hospital Association; Patel IS, Seemungal TA, Wilks M, Lloyd-Owen SJ, Donaldson GC, Wedzicha JA. Relationship between bacterial colonisation and the frequency, character, and severity of COPD exacerbations. Thorax 2002;57: Standardization of Spirometry, 1994 Update. American Thoracic Society. Am J Respir Crit Care Med 1995;152: Standard unit, evaluations and standards laboratory. Standard operating procedure for the investigation of sputum. BSOP8. Health Protection Agency, Standard Operating Procedures. Technical Services, PHLS HQ, UK, p Murray PR, Baron EJ, Jorgensen JH, Pfaller MA, Yolken RH. Manual of clinical microbiology, 8th ed. Washington, DC, USA: ASM Press; Chan CH, Cohen M, Pang J. A prospective study of community-acquired pneumonia in Hong Kong. Chest 1992;101: Department of Health of Hong Kong. Tuberculosis notifications (all forms) & rate by age and sex. gov.hk/dh/publicat/web/tb/tb2003e.htm Davies L, Angus RM, Calverley PM. Oral corticosteroids in patients admitted to hospital with exacerbations of chronic obstructive pulmonary disease: a prospective randomised controlled trial. Lancet 1999;354: Niewoehner DE, Erbland ML, Deupree RH, et al. Effect of systemic glucocorticoids on exacerbations of chronic obstructive pulmonary disease. Department of Veterans Affairs Cooperative Study Group. N Engl J Med 1999;340: Dooley KE, Golub J, Goes FS, Merz WG, Sterling TR. Empiric treatment of community-acquired pneumonia with fluoroquinolones, and delays in the treatment of tuberculosis. Clin Infect Dis 2002;34: Rossman MD. Colonization with mycobacterium avium complex an outdated concept. Eur Respir J 1999;13: Lode H, Schaberg T, Raffenberg M, Mauch H. Diagnostic problems in lower respiratory tract infections. J Antimicrob Chemother 1993;32(Suppl A): Murray PR, Washington JA. Microscopic and baceriologic analysis of expectorated sputum. Mayo Clin Proc 1975;50: Eller J, Ede A, Schaberg T, Niederman MS, Mauch H, Lode H. Infective exacerbations of chronic bronchitis: relation between bacteriologic etiology and lung function. Chest 1998;113: Monso E, Ruiz J, Rosell A, et al. Bacterial infection in chronic obstructive pulmonary disease. A study of stable and exacerbated outpatients using the protected specimen brush. Am J Respir Crit Care Med 1995;152: Burge S, Wedzicha JA. COPD exacerbations: definitions and classifications. Eur Respir J Suppl 2003;41:46s 53s. 30. Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease (COPD) and asthma. This official statement of the American Thoracic Society was adopted by the ATS Board of Directors, November Am Rev Respir Dis 1987;136: National Heart, Lung and Blood Institute, World Health Organisation. Global initiative for chronic obstructive lung disease. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: NHLBI/WHO Workshop, executive summary, Smith JA, Redman P, Woodhead MA. Antibiotic use in patients admitted with acute exacerbations of chronic obstructive pulmonary disease. Eur Respir J 1999;13: Anthonisen NR, Manfreda J, Warren CP, Hershfield ES, Harding GK, Nelson NA. Antibiotic therapy in exacerbations of chronic obstructive pulmonary disease. Ann Intern Med 1987;106: Connors Jr. AF, Dawson NV, Thomas C, et al. Outcomes following acute exacerbation of severe chronic obstructive lung disease. The SUPPORT investigators (Study to understand prognoses and preferences for outcomes and risks of treatments). Am J Respir Crit Care Med 1996;154: Ewig S, Torres A. Severe community-acquired pneumonia. Clin Chest Med 1999;20: Moine P, Vercken JB, Chevret S, Chastang C, Gajdos P. Severe community-acquired pneumonia. Etiology, epidemiology, and prognosis factors. French Study Group for Community- Acquired Pneumonia in the Intensive Care Unit. Chest 1994;105:

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